raising pups of urban san joaquin kit fox: relative roles of adult...

Western North American Naturalist 79(3), © 2019, pp. 364–377

Raising pups of urban San Joaquin kit fox: relative roles of adult group members

TORY L. WESTALL1,*, BRIAN L. CYPHER1, KATHERINE RALLS2, AND DAVID J. GERMANO3

1California State University, Stanislaus, Turlock, CA 95382 2Smithsonian Conservation Biology Institute, Washington, DC 200083California State University, Bakersfield, Bakersfield, CA 93311

ABSTRACT.—Maternal care of young is the norm in mammals because of internal gestation and lactation by females.Care by adults other than the mother is rare in most mammals but is common in primates, rodents, and carnivores. Westudied parental care in an urban population of the San Joaquin kit fox (Vulpes macrotis mutica), a small canid endemic tothe San Joaquin Desert in California. Kit fox family groups typically consist of a mated pair, the young-of-the-year, andoccasionally older offspring from previous years known as helpers. The relative contributions of the parents and helpersto the rearing of young are unknown in San Joaquin kit foxes. We determined the relative time investment (den atten-dance), the tasks performed (e.g., provisioning and guarding), and the chronology of participation and tasks performed byadult group members in pup rearing. We classified group members into 3 categories (mother, father, and helper) andmonitored them for 3 periods of the reproductive season (preparturition, nursing, and weaned). There was no differencein den attendance between periods, but there was a significant difference in den attendance by role. Mothers spent sig-nificantly more time at the den than either fathers or helpers. There was no significant difference between average provi-sioning events per hour per individual by role, but provisioning rates were significantly lower during the nursing periodcompared to the weaned period. Mothers provided the most direct care to young, while the role of fathers was primarilyto guard the family and maintain the territory. Assistance provided by helpers supplemented the efforts of the mother andfather and consisted primarily of guarding and some social interaction, especially play. Pups in groups with helpers wereleft unattended significantly less than pups in the group with no helpers, which may result in lower predation levels onpups. Helpers were likely tolerated because of a superabundance of food in the urban environment, but their presencemay reduce pup-rearing costs for parents and enhance the successful rearing of the current litter. Future research shouldcompare parental care in urban and nonurban kit foxes and determine whether helpers increase pup survival rates.

RESUMEN.—El cuidado materno de las crías es la norma en los animales mamíferos como consecuencia de lagestación interna y de la posterior lactancia. El cuidado por parte de adultos que no sean la madre es inusual en la may-oría de los mamíferos. Sin embargo, ocurre en primates, roedores y carnívoros. Analizamos el cuidado parental en unapoblación urbana de zorrita del desierto de San Joaquín (Vulpes macrotis mutica), pequeños cánidos endémicos deldesierto de San Joaquín en California. El grupo familiar de la zorrita del desierto se compone, típicamente, de la parejareproductiva, crías nacidas ese año y, en ocasiones, crías mayores conocidas como ayudantes. Desconocemos la contribu-ción relativa de los padres y de los ayudantes en la crianza de los cachorros, en la población de zorritas del desierto deSan Joaquín. Determinamos la inversión de tiempo (presencia en las madrigueras), las tareas realizadas (por ejemplo, elsuministro de alimentos y la vigilancia), la cronología de participación y la realización de tareas por los miembros adultosdel grupo en la crianza de los cachorros. Clasificamos a los miembros del grupo en tres categorías (madre, padre y ayu-dante) y los monitoreamos durante los tres períodos de la época reproductiva: preparto, lactancia y destete. No encon-tramos diferencias en cuanto a la presencia en las madrigueras entre los períodos, pero sí hubo una diferencia significativaen cuanto a la atención de las madrigueras por rol. Las madres pasaron considerablemente más tiempo en las madriguerasque los padres o los ayudantes. No hubo diferencias significativas en el promedio de eventos de provisión de alimentospor hora por individuo según el rol. Sin embargo, las tasas de suministro fueron más bajas durante el período de lactanciacomparadas con el período de destete. Las madres brindaron mayor atención directa a las crías, mientras que el papel delos padres fue principalmente el de proteger a la familia y preservar el territorio. La asistencia proporcionada por los ayu-dantes complementó los esfuerzos de la madre y del padre y consistió principalmente en la vigilancia y en cierta interac-ción social, especialmente durante el juego. Los cachorros en grupos con ayudantes significativamente permanecieron sinatención menos tiempo que aquellos en grupos sin ayudantes, lo que podría resultar en niveles menores de depredaciónde los cachorros. Es probable que los ayudantes fueran tolerados debido a la sobreabundancia de alimentos en el entornourbano, pero su presencia puede reducir los costos de la crianza para los padres y promover el éxito de la crianza de lacamada actual. Investigaciones futuras deberán comparar el cuidado parental de la zorrita del desierto de San Joaquín enambientes urbanos y no urbanos, para determinar si los ayudantes promueven la tasa de supervivencia de los cachorros.

*Corresponding author: [email protected]

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TLW orcid.org/0000-0002-4043-6752 BLC orcid.org/0000-0002-7349-545X

Maternal care of young is typical in mam-mals because of internal gestation and lacta-tion by females. Females typically investgreatly in offspring, while care of the young byother adults is relatively rare (Kleiman andMalcolm 1981, Clutton-Brock 1991, Woodroffeand Vincent 1994). Paternal care in mammalsis most common in primates, rodents, and car-nivores (Woodroffe and Vincent 1994). Pater-nal care occurs in about 40% of primate gen-era and has been described for many species(Muller and Thompson 2012, Huck and Fer-nandez-Duque 2013). There is also extensiveinformation on paternal care in small rodents(Dulac et al. 2014, Saltzman and Ziegler2014), but there are relatively few studies oncarnivores compared to those on primatesand rodents. Among carnivores, male parental care ismost common in canids, and fathers arethought to provide some form of care for theyoung in most species (Malcolm 1985). Canidyoung typically have a prolonged period ofdependence following birth, and in somespecies, pup survival is markedly enhancedby care from 2 parents versus a single parent(Macdonald et al. 2004). Parental care inmammals can be classified into direct andindirect behaviors (Kleiman and Malcolm1981). In canids, types of direct care includewatching for or defending young againstpredators; provisioning and attending young(remaining with young while other groupmembers forage); carrying, retrieving, groom-ing, and cleaning young; resting and hud-dling with young; and playing or socializingwith young. Indirect care includes den con-struction, alerting group members to danger,provisioning pregnant or lactating females,and territorial maintenance (Malcolm 1985). Alloparenting (i.e., care provided by adultsother than the mother or father) is also rela-tively rare in mammals, but common amongcanids (Macdonald and Sillero-Zubiri 2004).Such care is typically provided by young-of-the-year, who occasionally remain in theirnatal range and assist parents with rearingfuture litters (Moehlman 1989, Ralls et al.2001, Macdonald et al. 2004). Alloparentingby philopatric young has been described inblack-backed jackals (Canis mesomelas), Ethi -opian wolves (C. simensis), African wild dogs(Lycaon pictus) (Macdonald et al. 2004), goldenjackals (C. aureus), bat-eared foxes (Otocyon

megalotis) (Moehlman 1989), red foxes (Vulpesvulpes) (Soulsbury et al. 2010), swift foxes (V.velox) (Poessel and Gese 2013), and arcticfoxes (V. lagopus) (Elmhagen et al. 2014).While alloparenting is known to increasepup survival for black-backed jackals (Moehl -man 1989), evidence of the benefits of help -ers to pup survival in many other canidspecies is lacking (Macdonald et al. 2004).In many smaller foxes, such as swift and arc-tic foxes, the assistance provided by helpersdoes not seem to be substantial or necessary(Kruchenkova et al. 2009, Poessel and Gese2013). Although alloparenting can providemultiple benefits from an evolutionary per-spective (Moehlman 1989, Macdonald et al.2004), the behaviors and contributions ofhelpers have not been well described formost canid species. We studied San Joaquin kit foxes (V. macro-tis mutica), small canids that typically inhabitarid and semiarid habitats including desertscrub, chaparral, and native and nonnativegrasslands in central California (Macdonaldand Sillero-Zubiri 2004, Moehrenschlager etal. 2004, Cypher 2010). Unlike most othercanids, which only use dens for pup rearing,kit foxes use earthen or subterranean dens allyear (Koopman et al. 1998, Moehrenschlageret al. 2004, Cypher 2010). Dens are used toescape predators, to avoid temperature ex -tremes and water loss, for diurnal resting,and for pup rearing (Ralls and White 2003,Moehrenschlager et al. 2004, Cypher 2010).Kit foxes typically have multiple dens withintheir home range that are maintained byfamily groups (Morrell 1972, Ralls and White2003). A kit fox family group typically consistsof a mated pair and their current year’s off-spring (Ralls and White 2003, Cypher 2010).Occasionally, groups include additional adults(helpers) that are typically previous year’s off-spring, though this is rare and only occursapproximately 10% of the time in exurban kitfoxes (Ralls et al. 2001). Kit foxes are mostly monogamous, withoccasional cases of polygyny, and they gener-ally mate for life (Spiegel and Tom 1996,Moehrenschlager et al. 2004, Ralls et al.2007). They mate from late November toearly December, and young are born in densfrom late January to early March (Morrell1972, Moehrenschlager et al. 2004, Cypher2010). Litters consist of 1–7 pups, with an

WESTALL ET AL. ♦ URBAN SAN JOAQUIN KIT FOX PARENTAL CARE 365

average of 4 (Moehrenschlager et al. 2004,Ralls et al. 2007). Pups emerge from the denat 4 weeks, are weaned at 8 weeks, and becomeindependent at 5–6 months (Morrell 1972,Moehrenschlager et al. 2004, Ralls et al. 2007).At that time, young will either disperse orcontinue to occupy their natal ranges for vari-able time periods, and may even take over therange, usually when one or both parents die(Ralls et al. 2001, 2007, Cypher 2010). We observed San Joaquin kit foxes in Bak-ersfield, California, to determine the contri-butions of parents and helpers in pup rearing.Bakersfield (population 376,380) encompasses391 km2 with only 25% to 30% of its limitsabutting natural habitat (Cypher 2010). Never-theless, the city has a substantial populationof San Joaquin kit foxes living within its limits(Smith et al. 2006, Cypher 2010). The goals ofour study were to determine (1) the relativetime invested by each adult group memberin pup rearing, (2) the tasks performed byeach adult member in pup rearing (e.g., pro-visioning and guarding), and (3) the changesin adult behaviors over time as the pupsmatured. We hypothesized that parental carediffers among mothers, fathers, and helpers,predicting that mothers would provide themost direct care, fathers would provisionmore than other group members, and helperswould provide less care to pups than parents.Finally, we predicted that all group memberswould spend less time at the den in order toforage for more food as the pups grew olderand larger.

METHODS

Study Area

Bakersfield is located in the southeasternSan Joaquin Valley in Kern County, Califor-nia. Bakersfield is within the San JoaquinDesert and receives an average of 145 mm ofprecipitation between November and March,resulting in dry, hot summers and moist, coolwinters (Germano et al. 2011). Our study siteswithin Bakersfield were Stockdale HighSchool (SHS); California State University,Bakersfield (CSUB); and Bakersfield College(BC). We monitored family groups at schoolcampuses because ambient light was suffi-cient to observe foxes without the aid ofnight vision equipment. Additionally, foxes liv-ing on campuses were relatively accustomed

to human presence, not disturbed by the pres-ence of an observer, and observable withoutthe use of binoculars. Campuses were rela-tively safe and quiet at night so observationscould be conducted without interference. Alldens we monitored were located in landscap-ing beds and open manicured lawns.

Field Methods

We trapped foxes during late December2010 to mid-January 2011 and in early Janu-ary 2012 with wire-mesh box traps (38 × 38 ×107 cm; Tomahawk Live Trap, Hazelhurst,WI) that we baited with cat food, hot dogs,and sardines. We placed traps in secure loca-tions away from well-trafficked areas and cov-ered them with oiled cloth tarps to guardagainst the elements. We assessed each fox todetermine age, sex, and reproductive condi-tion and applied a uniquely numbered ear-tagto every individual. Females were ear-taggedon the right and males were ear-tagged onthe left to help distinguish sexes at a glance.Over the study, we collected hair samplesfrom all foxes for potential genetic analysis. Inaddition to hair samples, we began collectingtissue samples during the second year of thestudy when we realized that genetic analysiswould be necessary to determine parentagein some groups (Westall 2015). We collectedtissue samples from one ear using a 2-mmdisposable biopsy punch (Inegra® Miltex®,Model 33-31, York, PA) and stored them in95% ethanol. To determine individual contributions topup rearing, each adult fox in a family groupneeded to be easily identifiable. We markedeach fox with a unique pattern using a blackpermanent nontoxic dye (Nyanzol-D; AlbinalDyestuff, Inc., Jersey City, NJ) to allow for theidentification of individuals over the courseof the project. In addition to dye markings,we attached very high frequency (VHF) col-lars (Model E2C 162A; Sirtrack, HavelockNorth, New Zealand) to adult foxes in orderto locate foxes and dens. We only collaredadult foxes (>2 years old) that were exhibitingsigns of breeding (e.g., swollen vulva, enlargedtestes). The VHF signal could be tracked witha receiver (Communications Specialists, Inc.,Model R1000, Orange, CA) paired with a 3-element antenna (AF Antronics, Inc., ModelF150-3FB, Urbana, IL) or omnidirectionalantenna (Telonics, Model RA-5A, Mesa, AZ).

366 WESTERN NORTH AMERICAN NATURALIST (2019), VOL. 79 NO. 3, PAGES 364–377

Once we were reasonably sure that we hadcaptured most, if not all, adult foxes from afamily group, we began collecting data byconducting direct observations. During obser-vation sessions, we recorded times when adultfoxes were present and absent from the den,as well as behaviors performed above groundwhile foxes were at the den (Table 1). We alsonoted behaviors that we observed opportunis-tically while foxes were away from the den(Table 1). We observed the foxes at each denfor a 2-h session 1–2 times a week betweenJanuary and May in 2011 and 2012. Becausekit foxes are nocturnal and remain in under-ground dens during the day, we tracked tar-get foxes to the den they were currently usingat least 0.5 h prior to sunset. If adults weretracked to more than one den, the den withthe mother in it was observed, as this wasmost likely to be the natal den. After trackingfoxes to the den, we found a nearby locationwith a clear view of the den from which toconduct observations. Generally, these loca-tions were 30–50 m from the den, but therewas one group that was so accustomed tothe presence of humans that observers couldsit on a bench 10 m from the den, as thesefoxes behaved normally even with foot trafficoccurring within 3 m of the den. Our 2-h

observation session began as soon as a foxemerged from the den. We recorded the number of minutes thateach adult fox was present or absent fromthe den; foxes were considered present whenthey were in the den or above ground at theden. We divided the amount of time eachadult fox was present into 3 behavior cate-gories: time in the den, time performing carebehaviors above ground, and time perform-ing noncare behaviors above ground (careand noncare behaviors adapted from Klei -man and Malcolm 1981) (Table 1). Whileobserving the den, we recorded the numberof times each fox provisioned food at theden, as well as what item was provisioned if itcould be determined. We categorized foxes into 3 roles: mother,father, or helper. For family groups with femalehelpers, we initially used nursing behavior toidentify the mother. For one family groupwith a male helper, we used genetic analysis(Westall 2015) to determine which male wasthe father and which male was a helper. Weestimated the date of birth of the pups bycounting back 4 weeks from the date of emer-gence. To determine changes in behavior overtime, we divided the reproductive season into3 periods: preparturition, nursing, and weaned.


TABLE 1. Definitions of behaviors (adapted from Kleiman and Malcolm 1981) observed in San Joaquin kit foxes(Vulpes macrotis mutica) during the 2011 and 2012 reproductive seasons in Bakersfield, California, USA.

Behavior Definition

QUANTIFIED BEHAVIORS Den attendance Present Inside the den or present outside the den, including patrolling while pups were outside the den Absent Not present at the den Care behaviors Huddling Makes body contact with pups, such as cuddling or nursing Grooming Nibbles and/or licks pups to clean them Retrieving Calls pups to the den, herds pups to the den, or bodily retrieves pups and returns them to the den Guarding Watches over pups and/or patrols the area around the den to ensure safety Playing Initiates or engages in chasing or wrestling with pups Provisioning Provides food to the pregnant or lactating female and to pups Active defense Actively defends the den or pups from a perceived threat Den modification Digs at the den to remove waste or modify the den Noncare behaviors Socializing Interacts with other adults without the presence of pups Resting Rests or naps at the den without the presence of pupsOPPORTUNISTICALLY OBSERVED BEHAVIORS Resource maintenance Patrols throughout the territory, scent marking via urination and/or defecation Sentinel and antipredator behavior Patrols the territory looking for threats and actively defends the territory from intruders

Preparturition lasted from the start of obser-vations to the birth of the pups. The nursingperiod began at the estimated date of birthand ended at 8 weeks of age. The final period,weaned, began when the pups reached 8weeks of age and lasted until the pups beganto leave the den with their parents. Splittingthe breeding season into these 3 periodsallowed us to monitor changes in adult kit foxcontributions to pup rearing as the needs ofthe pups changed.

Statistical Analysis

We analyzed the amount of time adult foxeswere present (i.e., in the den and at the denabove ground) and absent (i.e., away from theden), as well as how much time was spentperforming care or noncare-related behaviorswhile at the den above ground. To determinerelative care contributions, we calculated theaverage number of minutes each fox was pres -ent per observation session. We standardizedobservation sessions to 2 h and used counts ofminutes for statistical analyses. A 2-way analy-sis of variance (ANOVA) was used to test fordifferences in the amount of time individualswere present by role and between periods, aswell as any interactions between role andperiod. Tukey’s pairwise comparisons with Pvalues adjusted for multiple comparisons wereused to determine differences between rolesand between periods. We treated groups withand without helpers the same, except whenanalyzing the amount of time dens were leftunattended. We analyzed the amount of timedens were left unattended overall and acrossperiods using a Kruskal–Wallis test with Pvalues adjusted for ties to compare betweenthe family groups with helpers and the familygroup without helpers. We used an arcsine transformation to nor-malize the proportion of time present that eachfox spent in the den, providing care whileabove ground (huddling, grooming, retrieving,guarding, playing, provisioning, den modifi-cation, and active defense), or performingnoncare-related behaviors while above ground(resting or socializing while pups were notpresent) (Table 1). We used a general linearmodel to test for differences in the proportionof time present by role, period, and behavior,as well as any interactions between role,period, and behavior. Tukey’s pairwise com-parisons with P values adjusted for multiple

comparisons were used to determine differ-ences in behavior between roles and betweenperiods. Behaviors observed while foxes werepresent were only compared between thenursing and weaned periods, because carecould not be provided during the preparturi-tion period. We summarized the number of provision-ing events per hour per individual by role in2-week increments to determine how provi-sioning events changed to meet the increas-ing energetic needs of the pups as theymatured. We used a Kruskal–Wallis test withP values adjusted for ties to compare the aver-age provisioning events per hour per individ-ual between periods, as well as between roles.We used Minitab (Minitab 17, Minitab Inc.,State College, PA) for all statistical analyses(a = 0.05 for all tests).

RESULTS

In 2011, we monitored one family groupfrom Bakersfield College (BC-2011) and onefamily group from Stockdale High School(SHS), and in 2012 we monitored one familygroup from Bakersfield College (BC-2012)and 2 family groups from California StateUniversity, Bakersfield (CSUB-S and CSUB-C) (Table 2). The SHS group did not producepups, so we were unable to include it in thisanalysis. Two helpers from the BC-2011 groupwere not captured and marked before thebreeding season began (6525 � and 6523 �)and our permits do not allow us to trap duringthe breeding season. Because these foxes wereindistinguishable, the individuals had to beexcluded from the analysis for this group. TheBC-2011 and BC-2012 groups were moni-tored at the same natal den during consecu-tive years, but the breeding pair from 2011both died of vehicle strikes before the 2012reproductive season. Two groups, BC-2012 andCSUB-S, had 2 mothers with communal lit-ters raised in the same den. Each group withcommunal litters was treated as a single fam-ily group. We used a total of 4 groups for allour analyses.

Den Attendance

The average proportion of time spent atthe den ranged from 43.2% to 67.4% formothers, from 20.0% to 32.4% for helpers,and from 9.5% to 14.5% for fathers. Kit foxes


spent significantly different amounts of timeat the den based on role (F2, 33 = 11.06, P <0.001), but similar amounts of time across the3 periods (F2, 33 = 1.46, P = 0.247). Therewas no significant interaction between roleand period (F4, 33 = 0.24, P = 0.913). Moth-ers spent significantly more time at the denthan helpers (t = 2.54, df = 8, P = 0.042)and fathers (t = 4.64, df = 8, P < 0.001; Fig.1). The amount of time that helpers andfathers spent at the den was not significantlydifferent (t = 1.92, df = 8, P = 0.148; Fig. 1).

The group without helpers left the natalden unattended significantly more than thegroups with helpers (H = 11.18, df = 1, P =0.001). On average, the group without helpersleft the natal den unattended 46.2% (median47.5%) of the time, while the groups withhelpers left the natal den unattended 18.3%(median 15.0%) of the time. There was no sig-nificant difference in the time that dens wereleft unattended across periods (H= 1.90, df = 2,P = 0.388).


TABLE 2. San Joaquin kit fox (Vulpes macrotis mutica) family group members and number of observation days duringthe 2011 and 2012 reproductive seasons in Bakersfield, California, USA. NA = not applicable.

Observation days No. Pups __________________________________Family group Mother Father Helper pups sampled Preparturition Nursing Weaned

BC-2011 6069� 6547� 6521� 3 6522� 6 14 13 6523�* 6524� 6525�* 6584� 6566�BC-2012 6566� 6524� 6584� 10 6595� 1 7 4 6525� 6596� 6606� 6607� 6677� 6678�CSUB-S 6700� 6065� 6585� 6 6593� 8 8 5 6309� 6594� 6676� U177CSUB-C 6592� 6578� NA 4 none 3 7 4*Individuals not included in statistical analyses

Fig. 1. Average number of minutes that adult San Joaquin kit foxes (Vulpes macrotis mutica) were present at the natalden by role during the 2011 and 2012 reproductive seasons in Bakersfield, California, USA. Vertical bars represent 95%confidence intervals.

Behavior While at the Den

Proportion of time spent performing eachbehavior differed (F2, 66 = 13.79, P < 0.001),but role (F2, 66 = 0.00, P = 1.000) and period(F1, 66 = 0.00, P = 1.000) were not significantfactors. There were also significant interac-tions between role and behavior (F4, 66 =7.97, P < 0.001) and between period andbehavior (F2, 66 = 11.42, P < 0.001). Mothersand helpers spent a significantly larger pro-portion of their time present in the den thanfathers did, while fathers spent a significantlylarger proportion of their time present pro-viding care above ground (Fig. 2). All adultgroup members spent a significantly largerproportion of time in the den when pupswere nursing and a larger proportion of timeproviding care above ground when pupswere weaned (Fig. 3). There were no signifi-cant interactions between role and period(F2, 66 = 0.00, P = 1.00) or between role,period, and behavior (F4, 66 = 1.37, P =0.254). All foxes spent significantly less timeperforming noncare behaviors (resting andsocializing) than they spent in the den (t =−3.20, df = 34, P = 0.006) or providing careat the den above ground (t = −5.21, df = 54,P < 0.001). The amount of time foxes spentin the den and providing care above grounddid not differ significantly (t = −2.00, df =54, P = 0.120).

The amount of time mothers spent in theden and at the den providing care did not dif-fer significantly, but mothers spent less timeperforming noncare behaviors than theyspent in the den or providing care aboveground at the den (Table 3). While presentat the den, fathers spent significantly moretime providing care above ground than in theden or performing noncare behaviors aboveground (Table 3). Fathers also spent a signifi-cantly larger proportion of their time whenpresent at the den providing care aboveground compared to helpers (Table 3). Theproportion of time at the den that helpersspent providing care above ground did notdiffer significantly from time in the den ortime performing noncare behaviors aboveground (Table 3). The amount of time allfoxes spent providing care above ground atthe den in the nursing period did not differsignificantly from time in the den or timeperforming noncare behaviors; however, therewas a significant difference in the amount of time foxes spent in the den and theamount of time they spent performing non-care behav iors (Table 3). During the weanedperiod, foxes spent significantly more of theirtime present providing care above ground atthe den than they spent in the den or per-forming noncare behaviors above ground atthe den (Table 3).


Fig. 2. Average number of minutes present at the natal den that adult San Joaquin kit fox (Vulpes macrotis mutica)mothers, fathers, and helpers spent in the den, providing care above ground, or performing noncare behaviors during the2011 and 2012 reproductive seasons in Bakersfield, California, USA. Vertical bars represent 95% confidence intervals.


Fig. 3. Average proportion of time present at the natal den that adult San Joaquin kit foxes (Vulpes macrotis mutica)spent in the den, providing care above ground, or performing noncare behaviors during the nursing period and theweaning period during the 2011 and 2012 reproductive seasons in Bakersfield, California, USA. Vertical bars represent95% confidence intervals.

TABLE 3. Tukey’s pairwise comparisons with adjusted P values analyzing differences in proportions of time that adultSan Joaquin kit foxes (Vulpes macrotis mutica) spent in the natal den or performing care- and noncare-related behaviorsabove ground at natal dens in Bakersfield, California, USA, during the nursing and weaned periods of the 2011 and 2012reproductive seasons.

Comparison df t P

Behavior within roles (father in the den) – (father care) 4 −5.17 <0.001 (father noncare) – (father care) 4 −5.52 <0.001 (father noncare) – (father in the den) 4 −0.35 1.000 (mother in the den) – (mother care) 4 0.36 1.000 (mother noncare) – (mother care) 4 −3.72 0.012 (mother noncare) – (mother in the den) 4 −4.09 0.004 (helper in the den) – (helper care) 4 1.60 0.801 (helper noncare) – (helper care) 4 0.05 1.000 (helper noncare) – (helper in the den) 4 −1.55 0.829Behavior between roles (mother in the den) – (father in the den) 4 3.09 0.068 (father in the den) – (helper in the den) 4 −2.66 0.184 (mother in the den) – (helper in the den) 4 0.18 1.000 (mother care) – (father care) 4 −2.90 0.107 (father care) – (helper care) 4 4.11 0.003 (mother care) – (helper care) 4 1.60 0.799 (mother noncare) – (father noncare) 4 −0.19 1.000 (father noncare) – (helper noncare) 4 −1.46 0.871 (mother noncare) – (helper noncare) 4 −1.78 0.693Behavior within periods (nursing in the den) – (nursing care) 2 1.81 0.467 (nursing noncare) – (nursing care) 2 −1.19 0.839 (nursing noncare) – (nursing in the den) 2 −3.00 0.042 (weaned in the den) – (weaned care) 2 −4.64 <0.001 (weaned noncare) – (weaned care) 2 −6.17 <0.001 (weaned noncare) – (weaned in the den) 2 −1.53 0.648Behavior between periods (nursing in the den) – (weaned in the den) 2 −2.64 0.102 (nursing care) – (weaned care) 2 −3.81 0.004 (nursing noncare) – (weaned noncare) 2 1.17 0.850

We observed 80 provisioning events, ofwhich 42 (52.5%) were by mothers, 29 (36.3%)were by fathers, and 9 (11.2%) were by helpers.Only a single provisioning event occurredduring preparturition, so data were only com-pared between the nursing and weaned peri-ods. Average provisioning events per hourper individual was not significantly differentbased on role (H = 2.86, df = 2, P = 0.240).The average number of provisioning eventsper hour per individual was significantlylower during the nursing period when com-pared to the weaned period (H = 5.39, df =1, P = 0.020). Provisioning events per hour

per individual by foxes of all roles increasedwhen the pups were fully weaned at 8 weeksof age (Fig. 4). Sample sizes were too small todetermine differences in provisioning ratesby role across periods. We documented kitfoxes provisioning many anthropogenic itemsincluding pizza, potato chips, fast food, andvarious refuse that had no nutritional value.Kit foxes also provided natural food itemsincluding desert cottontails (Sylvilagus audu -bonii), California ground squirrels (Otosper-mophilus beecheyi), rats (Rattus sp.), birds, andAmerican bullfrogs (Lithobates catesbeianus). Although some direct care behaviors wereperformed by foxes of all roles, others werenot (Table 4). Sample sizes were too small forstatistical analysis, so we only report trendsfor these data. Only mothers were observedhuddling with young, grooming young, andretrieving young. While mothers sometimesphysically retrieved pups, they also fre-quently herded them toward the den oralerted them to return to the den by barking.Only mothers and fathers engaged in activedefense of the pups by warding off per-ceived threats, such as cats or people. Onlyfathers and helpers were regularly observedplaying with the pups. Foxes of all roles wereobserved guarding and provisioning pups.Fathers were regularly seen away from theden urinating and defecating to mark the ter-ritory, and one father was observed warding


Fig. 4. Average provisioning events per hour per individual performed by San Joaquin kit fox (Vulpes macrotis mutica)mothers, fathers, and helpers as pups matured during the 2011 and 2012 reproductive seasons in Bakersfield, California,USA. Vertical bars represent standard errors.

TABLE 4. Direct and indirect care behaviors (afterKleiman and Malcolm 1981) performed by mother, father,and helper San Joaquin kit foxes (Vulpes macrotis mutica)during the 2011 and 2012 reproductive seasons in Bakers-field, California, USA.

Behavior Mother Father Helper

Direct care behaviors Huddling X Grooming X Retrieving X Guarding X X X Playing X X Provisioning X X X Active defense X X Indirect care behaviors Resource maintenance X Den modification X X X Sentinel and X anti-predator behavior

Aver

age

Prov

isio

ning

Even

ts p

er H

our p

er In

divi

dual

Pup Age in Weeks

off a red fox that had entered the territory.Foxes of all roles performed den maintenanceand modifications by digging and cleaning outthe entrances throughout the breeding season.

DISCUSSION

Parental Care by Role

While all individuals in the study providedsome level of care to pups, their role was themost relevant factor in predicting the typesand amount of care provided. Mothers spentmore time at the den than other family mem-bers and provided the most direct care tothe pups. Mothers were the only family mem-bers to huddle with pups, groom them, andretrieve them when they were too far fromthe den. Behaviors that were performed bymothers as well as other group membersincluded guarding pups, defending the denfrom threats, and provisioning pups with food.Mothers guarded the young by vigilantlywatching the pups and the surrounding area,and they frequently patrolled around the denin wide circles, stopping at regular intervalsto scan the area. If a threat was perceived,the mother would vocalize a warning and thepups would immediately return to the den.Perceived threats included cats, dogs, andhumans (e.g., students, security staff, groundskeepers). Occasionally, mothers would activelydefend the den from cats and humans bystalking them until they were out of the area,but at other times they would simply wait forthe threat to pass and would then signal, pre-sumably through vocalization, for the pups toexit the den again. The only direct care behavior that moth-ers did not regularly perform was play. Moth-ers rarely played with pups and sometimesaggressively bit them if they persistentlytried to initiate play. Mothers modified densbut were not seen performing other indirectcare behaviors, such as resource maintenance(e.g., scent-marking the territory) or sentineland antipredator behavior, which would haverequired being away from the den. It is note-worthy that foxes of all roles performed denmaintenance, as it has been suggested thatden construction in other canids is performedexclusively by breeding females (Malcolm 1985). Fathers spent significantly less time at theden than mothers, but most of their time atthe den was spent providing care to the pups.

Fathers primarily guarded pups, activelydefended the den, and provisioned mothersand pups. While guarding pups at the den,fathers exhibited the same vigilance as moth-ers; however, they defended the territorymore frequently and more aggressively thanmothers. One father was observed snarlingand growling at a red fox that had wanderedinto the territory near the natal den. Redfoxes, which are considerably larger than kitfoxes, have been documented killing adult kitfoxes (White and Ralls 1993, Clark et al.2005) and are known to limit reproductivesuccess in arctic foxes by killing their pups(Hersteinsson and Macdonald 1992, Tanner-feldt et al. 2002). Nevertheless, the father inthis group continued his aggressive behavioruntil the red fox left the area. The onlydirect care behavior that fathers performedmore frequently than mothers was playingwith the pups. Indirect care behaviors per-formed by fathers included maintaining theterritory through urination and defecation,den modification, and sentinel and antipreda-tor behavior away from the den. Male kitfoxes are known to scent mark more thanfemales, and a greater proportion of theirmarks are in boundary areas of home ranges(Murdoch 2004). Although helpers are sometimes found innonurban populations (Koopman et al. 2000,Ralls et al. 2001, Moehrenschlager et al.2004), they are much less common than inthe Bakersfield population (Cypher 2010).Only about 10% of the mated pairs in exur-ban environments have helpers (Ralls et al.2001), whereas helpers were present in 3 ofthe 4 groups we monitored. Not only didmost of our groups have helpers present, butone group had 4 helpers. The abundant foodsupply in Bakersfield ensures that most matedpairs can share their territories with one ormore other adults at little or no cost to them-selves or their future litters. Helpers spent significantly less time at theden than mothers, but not fathers. Althoughfathers and helpers spent similar amounts oftime at the den, helpers spent significantlyless time providing care to pups than fathers.Most of the time helpers spent at the denwas spent resting, although occasionally theywould guard the pups or provision them.Helpers were never observed actively defend-ing the den or the territory. When guarding,


helpers tended to be less vigilant than moth-ers and fathers, sometimes playing with pupsinstead of watching them. Playing with the pups was the only directcare behavior that helpers seemed to performmore than other roles. Play is an importantpreparation for adult life (Bekoff 1995), andthe father in the group with no helpers playedwith the pups, whereas in the other groups itwas mostly the helpers that played with pups.The frequent presence of the helper(s) at theden may have enabled the parents, especiallythe fathers in these groups, to spend less timeplaying with pups at the den, freeing them forother activities. Play between individuals canalso serve to establish dominance (Cordoni2009). As kit foxes can breed at 1 year of age(Cypher et al. 2000), a pup can potentiallytake over the territory of its parent the follow-ing reproductive season. It may be importantfor the helpers to establish dominance overthe pups in the event an opportunity arises totake over the territory. Although helpers provided little direct carefor the pups, they often attended them whileneither parent was present. Groups withhelpers left the den unattended for less timethan the group without helpers, so helpersmay increase pup survival by reducing theopportunity for predation on pups. Only 2pups died during the course of our study, oneto raptor predation and one to unknown causes,so we did not have sufficient data to deter-mine the effect of helpers on pup survival. Itis also worth noting that behavior occurringinside the den could not be observed, and thatthere may therefore be other direct carebehaviors performed by helpers. The only indi-rect care behavior that helpers were observedperforming was den modification. While the exact benefits of helpers arehard to define, there are some potential bene-fits documented in kit foxes. Helpers provideinsurance for the breeding pair and theirfuture offspring. In the event that one of thebreeding pair dies, helpers are potentialmates for the breeding adult of the oppositesex. When this adult is the parent of thehelper, inbreeding can result, but it has none -theless been documented in this urban kitfox population (Westall 2015). Helpers couldalso potentially care for the pups if somethinghappened to either or both of the parents. Kitfox helpers sometimes adopt and raise pups

following the death of a parent (Spiegel andTom 1996). Finally, helpers could also poten-tially benefit the mated pair if they inherit theterritory and produce offspring related to thepair.

Behavioral Changes Over the Reproductive Season

Den attendance patterns by role did notchange, and there was no difference in theamount of time the pups were left unat-tended while above ground as the pups grewolder. When pups first emerged, one or moreadult foxes were usually present at the denwhen pups were above ground, and pupswould go back into the den almost immedi-ately when an adult fox left the area. As thepups grew older, the frequency and durationof periods where the pups were left un -attended increased, but this was a result ofpups spending more time above ground ratherthan the den being left unattended for longerperiods of time. Behaviors of adults whilethey were present at the den did change.During the nursing period, adult group mem-bers spent a larger proportion of their timepresent in the den. During the weaningperiod, adults spent more of the their timepresent providing care above ground. Whilepups were younger and more vulnerable,adults would stay in the den, presumably toprovide care; then, as the pups grew olderand spent more time out of the den, care tookplace above ground. There was a noticeable change in provi-sioning events as the pups matured. Thenumber of provisioning events per individualper hour surged during the weaned periodcompared to the nursing period. Kit fox pupsare fully weaned after 8 weeks, and becausepups no longer receive nutrition via lactation,but are not old enough to hunt for them-selves, parents are required to bring morefood to the den to meet the growing ener-getic demands of pups. During this time,provisioning events increased markedly, butby 14 weeks of age, pups began venturing far-ther from the den, and at that point provi-sioning at the den tapered off.

Comparisons to Other Fox Species

In general, our den attendance observationson kit foxes were consistent with observa-tions on other socially monogamous fox species,


although there were some differences. As inmost other monogamous canids, includingswift (Poessel and Gese 2013), arctic (Garrottet al. 1984, Strand et al. 2000), and red foxes(Vergara 2001, Soulsbury et al. 2010), breed-ing females spent the most time with pupsand also provided the most direct care, whilebreeding males spent little time at the denbut spent considerable time foraging to provi-sion pups and lactating females. Den atten-dance patterns of kit foxes did differ com-pared to patterns of the similarly sized bat-earedfoxes, but this is likely related to availableprey. Bat-eared fox males spent significantlymore time with pups than mothers did, andmales also performed many of the behaviorsthat female kit foxes perform, such as guard-ing, huddling, playing, retrieving, and groom-ing offspring (Maas and Macdonald 2004,Wright 2006). Bat-eared foxes rely primarilyon insects for food, and lactating females mustspend large portions of the night away fromthe den to obtain enough nutrients to pro -duce milk as well as meet their own energeticneeds (Maas and Macdonald 2004, Wright2006). In contrast, because kit foxes rely pri-marily on rodents in exurban environmentsand on relatively large prey and anthropo -genic food items in urban environments, adultsare able to forage for food that can easily bebrought to the den to provision pups and lac-tating females. In our study, den attendance patternsremained the same throughout the breedingseason, but different trends have been re -corded for swift foxes, which are an ecologi-cally similar species. Male swift foxes did notchange their den attendance patterns overthe course of the breeding season, althoughfemales did (Poessel and Gese 2013). Femaleswift foxes spent more time with pups earlyin the breeding season and spent less time atthe den as the pups grew older, probablybecause of the high consumption of insectsby adults later in the breeding season (Poes-sel and Gese 2013). Because insects cannotbe carried back to the pups, adult swift foxesregurgitated food for their offspring (Poesseland Gese 2013), a behavior that has not beendocumented in kit foxes. It is likely thatfemale kit foxes in our study were able tospend a relatively constant amount of timewith the pups because the ample and consis-tent supply of resources in the urban envi-

ronment allows females to gather the neces-sary nutrients for producing milk in a rela-tively short amount of time. Fathers also pro-vided food items for both pups and mothers,allowing mothers to remain at the den to pro-vide direct care to their offspring throughoutthe breeding season. The increased frequency of helpers andthe greater number of helpers per group inthe urban environment seems to be consistentwith observations on other species, though alarger sample size is required for a statisticalanalysis. Arctic foxes accept additional familymembers in years of high prey availability(Strand et al. 2000) and live in groups morefrequently when food availability increases,either naturally or with supplemental feed-ing (Elmhagen et al. 2014). Red foxes havealso been documented with higher occur-rences of philopatric young when resourceavailability and habitat stability are high(Gosselink et al. 2010). Similar to kit foxes, helpers in other species,including arctic foxes (Strand et al. 2000),Blanford’s foxes (Vulpes cana; Geffen and Mac-donald 1992), and red foxes (von Schantz1984), seem to provide little or no care to thepups but are still tolerated due to potentialbenefits to the breeding pair. The presence ofhelpers benefits the long-term reproductivesuccess of the breeding female in arctic foxes(Kruchenkova et al. 2009). The presence ofhelpers may also increase pup survival byreducing the amount of time the natal den isleft unguarded. Erlandsson et al. (2017) foundthat arctic fox pup survival was negativelycorrelated with the proportion of time pupswere left unattended. In our study, the pres-ence of helpers decreased the amount of timethe den was left unattended and may havereduced the predation risk to the pups. This is the first study to document par -ental care behaviors in the San Joaquin kitfox. The enhanced observability of kit foxesin the urban environment provided a goodopportunity to obtain detailed data on par -ental and alloparental care. Future researchcould compare parental care between urbanand exurban kit foxes. Questions of particularinterest include determining whether help -ers increase the survival of pups and whethergroup composition (particularly the presenceof helpers) varies with natural fluctuations inresource availability.


ACKNOWLEDGMENTS

We thank the Bureau of Land Managementfor financial support to refurbish collars andThe Western Section and the San JoaquinValley Chapter of The Wildlife Society andthe Student Research Scholar Program ofCalifornia State University, Bakersfield, forproviding grants to purchase equipment. Wethank Carl Kloock for reviewing an earlierdraft of the manuscript and all the individu-als who assisted in data collection and analy-ses for this project: S. Westall, S.E. Soles,S.W. Soles, C. Reedy, K. Reedy, R. Reedy, C.Van Horn Job, E. Kelly, M. Naderhoff, E. dela Rosa, E. Tennant, and A. Madrid. All trap-ping efforts were conducted in accordancewith a Memorandum of Understanding (#SC-003862) from the California Department ofFish and Wildlife, a federal permit to handleendangered species (#TE-825573) from theUnited States Fish and Wildlife Service, andan Institutional Animal Care and Use Com-mittee protocol (#10-02) from California StateUniversity, Bakersfield. Helpful suggestionsto improve the manuscript were provided byR. Erlandsson and an anonymous reviewer.

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Received 9 April 2018Revised 4 March 2019

Accepted 14 March 2019Published online 11 September 2019

raising pups of urban san joaquin kit fox: relative roles of adult...

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